Cortical Organization of Centrifugal Afferents to the Olfactory Bulb: Mono-and Trans-synaptic Tracing with Recombinant Neurotropic Viral Tracers
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摘要
Sensory processing is strongly modulated by different brain and behavioral states,and this is based on the top-down modulation.In the olfactory system,local neural circuits in the olfactory bulb(OB)are innervated by centrifugal afferents in order to regulate the processing of olfactory information in the OB under different behavioral states.The purpose of the present study was to explore the organization of neural networks in olfactory-related cortices and modulatory nuclei that give rise to direct and indirect innervations to the glomerular layer(GL)of the OB at the whole-brain scale.Injection of different recombinant attenuated neurotropic viruses into the GL showed that it received direct inputs from each layer in the OB,centrifugal inputs from the ipsilateralanterior olfactory nucleus(AON),anterior piriform cortex(Pir),and horizontal limb of diagonal band of Broca(HDB),and various indirect inputs from bilateral cortical neurons in the AON,Pir,amygdala,entorhinal cortex,hippocampus,HDB,dorsal raphe,median raphe and locus coeruleus.These results provide a circuitry basis that will help further understand the mechanism by which olfactory informationprocessing in the OB is regulated.
Sensory processing is strongly modulated by different brain and behavioral states,and this is based on the top-down modulation.In the olfactory system,local neural circuits in the olfactory bulb(OB)are innervated by centrifugal afferents in order to regulate the processing of olfactory information in the OB under different behavioral states.The purpose of the present study was to explore the organization of neural networks in olfactory-related cortices and modulatory nuclei that give rise to direct and indirect innervations to the glomerular layer(GL)of the OB at the whole-brain scale.Injection of different recombinant attenuated neurotropic viruses into the GL showed that it received direct inputs from each layer in the OB,centrifugal inputs from the ipsilateralanterior olfactory nucleus(AON),anterior piriform cortex(Pir),and horizontal limb of diagonal band of Broca(HDB),and various indirect inputs from bilateral cortical neurons in the AON,Pir,amygdala,entorhinal cortex,hippocampus,HDB,dorsal raphe,median raphe and locus coeruleus.These results provide a circuitry basis that will help further understand the mechanism by which olfactory informationprocessing in the OB is regulated.
Sensory processing is strongly modulated by different brain and behavioral states,and this is based on the top-down modulation.In the olfactory system,local neural circuits in the olfactory bulb(OB)are innervated by centrifugal afferents in order to regulate the processing of olfactory information in the OB under different behavioral states.The purpose of the present study was to explore the organization of neural networks in olfactory-related cortices and modulatory nuclei that give rise to direct and indirect innervations to the glomerular layer(GL)of the OB at the whole-brain scale.Injection of different recombinant attenuated neurotropic viruses into the GL showed that it received direct inputs from each layer in the OB,centrifugal inputs from the ipsilateralanterior olfactory nucleus(AON),anterior piriform cortex(Pir),and horizontal limb of diagonal band of Broca(HDB),and various indirect inputs from bilateral cortical neurons in the AON,Pir,amygdala,entorhinal cortex,hippocampus,HDB,dorsal raphe,median raphe and locus coeruleus.These results provide a circuitry basis that will help further understand the mechanism by which olfactory informationprocessing in the OB is regulated.
引文
1.Zhang S,Xu M,Kamigaki T,Hoang Do JP,Chang WC,Jenvay S,et al.Selective attention.Long-range and local circuits for topdown modulation of visual cortex processing.Science 2014,345:660-665.
2.McIntyre JC,Thiebaud N,McGann JP,Komiyama T,Rothermel M.Neuromodulation in chemosensory pathways.Chem Senses2017,42:375-379.
3.Padmanabhan K,Osakada F,Tarabrina A,Kizer E,Callaway EM,Gage FH,et al.Diverse representations of olfactory information in centrifugal feedback projections.J Neurosci2016,36:7535-7545.
4.D’Souza RD,Vijayaraghavan S.Paying attention to smell:cholinergic signaling in the olfactory bulb.Front Synaptic Neurosci 2014,6:21.
5.Fletcher ML,Chen WR.Neural correlates of olfactory learning:Critical role of centrifugal neuromodulation.Learn Mem 2010,17:561-570.
6.Markopoulos F,Rokni D,Gire DH,Murthy VN.Functional properties of cortical feedback projections to the olfactory bulb.Neuron 2012,76:1175-1188.
7.Imai T.Construction of functional neuronal circuitry in the olfactory bulb.Semin Cell Dev Biol 2014,35:180-188.
8.Uchida N,Poo C,Haddad R.Coding and transformations in the olfactory system.Annu Rev Neurosci 2014,37:363-385.
9.Takahashi H,Ogawa Y,Yoshihara S,Asahina R,Kinoshita M,Kitano T,et al.A subtype of olfactory bulb interneurons is required for odor detection and discrimination behaviors.J Neurosci 2016,36:8210-8227.
10.Grimaud J,Lledo PM.Illuminating odors:when optogenetics brings to light unexpected olfactory abilities.Learn Mem 2016,23:249-254.
11.Oswald AM,Urban NN.There and back again:the corticobulbar loop.Neuron 2012,76:1045-1047.
12.Otazu GH,Chae H,Davis MB,Albeanu DF.Cortical feedback decorrelates olfactory bulb output in awake mice.Neuron 2015,86:1461-1477.
13.Linster C,Cleland TA.Neuromodulation of olfactory transformations.Curr Opin Neurobiol 2016,40:170-177.
14.Lizbinski KM,Dacks AM.Intrinsic and extrinsic neuromodulation of olfactory processing.Front Cell Neurosci 2017,11:424.
15.Rothermel M,Wachowiak M.Functional imaging of cortical feedback projections to the olfactory bulb.Front Neural Circuits2014,8:73.
16.Manella LC,Petersen N,Linster C.Stimulation of the locus ceruleus modulates signal-to-noise ratio in the olfactory bulb.J Neurosci 2017,37:11605-11615.
17.Case DT,Burton SD,Gedeon JY,Williams SG,Urban NN,Seal RP.Layer-and cell type-selective co-transmission by a basal forebrain cholinergic projection to the olfactory bulb.Nat Commun 2017,8:652.
18.Wachowiak M,Economo MN,Diaz-Quesada M,Brunert D,Wesson DW,White JA,et al.Optical dissection of odor information processing in vivo using GCaMPs expressed in specified cell types of the olfactory bulb.J Neurosci 2013,33:5285-5300.
19.Burton SD.Inhibitory circuits of the mammalian main olfactory bulb.J Neurophysiol 2017,118:2034-2051.
20.Luo L,Callaway EM,Svoboda K.Genetic dissection of neural circuits.Neuron 2008,57:634-660.
21.Thorne RG,Emory CR,Ala TA,Frey WH,2nd.Quantitative analysis of the olfactory pathway for drug delivery to the brain.Brain Res 1995,692:278-282.
22.Callaway EM.Transneuronal circuit tracing with neurotropic viruses.Curr Opin Neurobiol 2008,18:617-623.
23.Nassi JJ,Cepko CL,Born RT,Beier KT.Neuroanatomy goes viral!Front Neuroanat 2015,9:80.
24.Bienkowski MS,Wendel ES,Rinaman L.Organization of multisynaptic circuits within and between the medial and the central extended amygdala.J Comp Neurol 2013,521:3406-3431.
25.Callaway EM,Luo L.Monosynaptic circuit tracing with glycoprotein-deleted rabies viruses.J Neurosci 2015,35:8979-8985.
26.Willhite DC,Nguyen KT,Masurkar AV,Greer CA,Shepherd GM,Chen WR.Viral tracing identifies distributed columnar organization in the olfactory bulb.Proc Natl Acad Sci USA 2006,103:12592-12597.
27.Kikuta S,Sato K,Kashiwadani H,Tsunoda K,Yamasoba T,Mori K.From the Cover:Neurons in the anterior olfactory nucleus pars externa detect right or left localization of odor sources.Proc Natl Acad Sci USA 2010,107:12363-12368.
28.Esquivelzeta Rabell J,Mutlu K,Noutel J,Martin Del Olmo P,Haesler S.Spontaneous rapid odor source localization behavior requires interhemispheric communication.Curr Biol 2017,27:1542-1548 e1544.
29.Wilson DA,Sullivan RM.Cortical processing of odor objects.Neuron 2011,72:506-519.
30.Tye KM,Deisseroth K.Optogenetic investigation of neural circuits underlying brain disease in animal models.Nat Rev Neurosci 2012,13:251-266.
31.Spehr M,Spehr J,Ukhanov K,Kelliher KR,Leinders-Zufall T,Zufall F.Parallel processing of social signals by the mammalian main and accessory olfactory systems.Cell Mol Life Sci 2006,63:1476-1484.
32.Sewards TV,Sewards MA.Input and output stations of the entorhinal cortex:superficial vs.deep layers or lateral vs.medial divisions?Brain Res Brain Res Rev 2003,42:243-251.
33.Shipley MT,Ennis M.Functional organization of olfactory system.J Neurobiol 1996,30:123-176.
34.Ke MT,Fujimoto S,Imai T.SeeDB:a simple and morphologypreserving optical clearing agent for neuronal circuit reconstruction.Nat Neurosci 2013,16:1154-1161.
35.De Saint Jan D,Hirnet D,Westbrook GL,Charpak S.External tufted cells drive the output of olfactory bulb glomeruli.J Neurosci 2009,29:2043-2052.
36.Liu S,Plachez C,Shao Z,Puche A,Shipley MT.Olfactory bulb short axon cell release of GABA and dopamine produces a temporally biphasic inhibition-excitation response in external tufted cells.J Neurosci 2013,33:2916-2926.
37.Kiyokage E,Pan YZ,Shao Z,Kobayashi K,Szabo G,Yanagawa Y,et al.Molecular identity of periglomerular and short axon cells.J Neurosci 2010,30:1185-1196.
38.Gire DH,Franks KM,Zak JD,Tanaka KF,Whitesell JD,Mulligan AA,et al.Mitral cells in the olfactory bulb are mainly excited through a multistep signaling path.J Neurosci 2012,32:2964-2975.
39.Murphy GJ,Darcy DP,Isaacson JS.Intraglomerular inhibition:signaling mechanisms of an olfactory microcircuit.Nat Neurosci2005,8:354-364.
40.Najac M,Sanz Diez A,Kumar A,Benito N,Charpak S,De Saint Jan D.Intraglomerular lateral inhibition promotes spike timing variability in principal neurons of the olfactory bulb.J Neurosci2015,35:4319-4331.
41.Parsa PV,D’Souza RD,Vijayaraghavan S.Signaling between periglomerular cells reveals a bimodal role for GABA in modulating glomerular microcircuitry in the olfactory bulb.Proc Natl Acad Sci U S A 2015,112:9478-9483.
42.Liu S,Puche AC,Shipley MT.The interglomerular circuit potently inhibits olfactory bulb output neurons by both direct and indirect pathways.J Neurosci 2016,36:9604-9617.
43.Banerjee A,Marbach F,Anselmi F,Koh MS,Davis MB,Garcia da Silva P,et al.An interglomerular circuit gates glomerular output and implements gain control in the mouse olfactory bulb.Neuron 2015,87:193-207.
44.Burton SD,LaRocca G,Liu A,Cheetham CE,Urban NN.Olfactory bulb deep short-axon cells mediate widespread inhibition of tufted cell apical dendrites.J Neurosci 2017,37:1117-1138.
45.Eyre MD,Antal M,Nusser Z.Distinct deep short-axon cell subtypes of the main olfactory bulb provide novel intrabulbar and extrabulbar GABAergic connections.J Neurosci 2008,28:8217-8229.
46.Pressler RT,Strowbridge BW.Blanes cells mediate persistent feedforward inhibition onto granule cells in the olfactory bulb.Neuron 2006,49:889-904.
47.Eyre MD,Kerti K,Nusser Z.Molecular diversity of deep shortaxon cells of the rat main olfactory bulb.Eur J Neurosci 2009,29:1397-1407.
48.Kelsch W,Sim S,Lois C.Watching synaptogenesis in the adult brain.Annu Rev Neurosci 2010,33:131-149.
49.Belluscio L,Lodovichi C,Feinstein P,Mombaerts P,Katz LC.Odorant receptors instruct functional circuitry in the mouse olfactory bulb.Nature 2002,419:296-300.
50.Lodovichi C,Belluscio L,Katz LC.Functional topography of connections linking mirror-symmetric maps in the mouse olfactory bulb.Neuron 2003,38:265-276.
51.Brunjes PC,Illig KR,Meyer EA.A field guide to the anterior olfactory nucleus(cortex).Brain Res Brain Res Rev 2005,50:305-335.
52.Yan Z,Tan J,Qin C,Lu Y,Ding C,Luo M.Precise circuitry links bilaterally symmetric olfactory maps.Neuron 2008,58:613-624.
53.Illig KR,Eudy JD.Contralateral projections of the rat anterior olfactory nucleus.J Comp Neurol 2009,512:115-123.
54.Boyd AM,Sturgill JF,Poo C,Isaacson JS.Cortical feedback control of olfactory bulb circuits.Neuron 2012,76:1161-1174.
55.Insausti R,Herrero MT,Witter MP.Entorhinal cortex of the rat:cytoarchitectonic subdivisions and the origin and distribution of cortical efferents.Hippocampus 1997,7:146-183.
56.de la Rosa-Prieto C,Ubeda-Banon I,Mohedano-Moriano A,ProSistiaga P,Saiz-Sanchez D,Insausti R,et al.Subicular and CA1hippocampal projections to the accessory olfactory bulb.Hippocampus 2009,19:124-129.
57.de Olmos J,Hardy H,Heimer L.The afferent connections of the main and the accessory olfactory bulb formations in the rat:an experimental HRP-study.J Comp Neurol 1978,181:213-244.
58.van Groen T,Wyss JM.Extrinsic projections from area CA1 of the rat hippocampus:olfactory,cortical,subcortical,and bilateral hippocampal formation projections.J Comp Neurol 1990,302:515-528.
59.Devore S,de Almeida L,Linster C.Distinct roles of bulbar muscarinic and nicotinic receptors in olfactory discrimination learning.J Neurosci 2014,34:11244-11260.
60.Bendahmane M,Ogg MC,Ennis M,Fletcher ML.Increased olfactory bulb acetylcholine bi-directionally modulates glomerular odor sensitivity.Sci Rep 2016,6:25808.
61.Hamamoto M,Kiyokage E,Sohn J,Hioki H,Harada T,Toida K.Structural basis for cholinergic regulation of neural circuits in the mouse olfactory bulb.J Comp Neurol 2017,525:574-591.
62.Gracia-Llanes FJ,Crespo C,Blasco-Ibanez JM,Nacher J,Varea E,Rovira-Esteban L,et al.GABAergic basal forebrain afferents innervate selectively GABAergic targets in the main olfactory bulb.Neuroscience 2010,170:913-922.
63.Nunez-Parra A,Maurer RK,Krahe K,Smith RS,Araneda RC.Disruption of centrifugal inhibition to olfactory bulb granule cells impairs olfactory discrimination.Proc Natl Acad Sci U S A 2013,110:14777-14782.
64.Escanilla O,Arrellanos A,Karnow A,Ennis M,Linster C.Noradrenergic modulation of behavioral odor detection and discrimination thresholds in the olfactory bulb.Eur J Neurosci2010,32:458-468.
65.Escanilla O,Alperin S,Youssef M,Ennis M,Linster C.Noradrenergic but not cholinergic modulation of olfactory bulb during processing of near threshold concentration stimuli.Behav Neurosci 2012,126:720-728.
66.Doucette W,Milder J,Restrepo D.Adrenergic modulation of olfactory bulb circuitry affects odor discrimination.Learn Mem2007,14:539-547.
67.Li G,Linster C,Cleland TA.Functional differentiation of cholinergic and noradrenergic modulation in a biophysical model of olfactory bulb granule cells.J Neurophysiol 2015,114:3177-3200.
68.Zhou FW,Dong HW,Ennis M.Activation of beta-noradrenergic receptors enhances rhythmic bursting in mouse olfactory bulb external tufted cells.J Neurophysiol 2016,116:2604-2614.
69.Gire DH,Schoppa NE.Long-term enhancement of synchronized oscillations by adrenergic receptor activation in the olfactory bulb.J Neurophysiol 2008,99:2021-2025.
70.Zhong W,Li Y,Feng Q,Luo M.Learning and stress shape the reward response patterns of serotonin neurons.J Neurosci 2017,37:8863-8875.
71.Fonseca MS,Murakami M,Mainen ZF.Activation of dorsal raphe serotonergic neurons promotes waiting but is not reinforcing.Curr Biol 2015,25:306-315.
72.Liu ZX,Zhou JF,Li Y,Hu F,Lu Y,Ma M,et al.Dorsal raphe neurons signal reward through 5-HT and glutamate.Neuron2014,81:1360-1374.
73.Liu Y,Jiang Y,Si Y,Kim JY,Chen ZF,Rao Y.Molecular regulation of sexual preference revealed by genetic studies of5-HT in the brains of male mice.Nature 2011,472:95-99.
74.Kraus C,Castren E,Kasper S,Lanzenberger R.Serotonin and neuroplasticity-Links between molecular,functional and structural pathophysiology in depression.Neurosci Biobehav Rev 2017,77:317-326.
75.Luo MM,Li Y,Zhong WX.Do dorsal raphe 5-HT neurons encode‘‘beneficialness’’?Neurobiol Learn Mem 2016,135:40-49.
76.Miyazaki KW,Miyazaki K,Tanaka KF,Yamanaka A,Takahashi A,Tabuchi S,et al.Optogenetic activation of dorsal raphe serotonin neurons enhances patience for future rewards.Curr Biol2014,24:2033-2040.
77.Huang Z,Thiebaud N,Fadool DA.Differential serotonergic modulation across the main and accessory olfactory bulbs.J Physiol 2017,595:3515-3533.
78.Steinfeld R,Herb JT,Sprengel R,Schaefer AT,Fukunaga I.Divergent innervation of the olfactory bulb by distinct raphe nuclei.J Comp Neurol 2015,523:805-813.
79.Liu SL,Aungst JL,Puche AC,Shipley MT.Serotonin modulates the population activity profile of olfactory bulb external tufted cells.J Neurophysiol 2012,107:473-483.
80.Brill J,Shao Z,Puche AC,Wachowiak M,Shipley MT.Serotonin increases synaptic activity in olfactory bulb glomeruli.J Neurophysiol 2016,115:1208-1219.
81.Schmidt LJ,Strowbridge BW.Modulation of olfactory bulb network activity by serotonin:synchronous inhibition of mitral cells mediated by spatially localized GABAergic microcircuits.Learn Mem 2014,21:406-416.
82.Petzold GC,Hagiwara A,Murthy VN.Serotonergic modulation of odor input to the mammalian olfactory bulb.Nat Neurosci2009,12:784-791.
83.Brunert D,Tsuno Y,Rothermel M,Shipley MT,Wachowiak M.Cell-type-specific modulation of sensory responses in olfactory bulb circuits by serotonergic projections from the raphe nuclei.J Neurosci 2016,36:6820-6835.
2.McIntyre JC,Thiebaud N,McGann JP,Komiyama T,Rothermel M.Neuromodulation in chemosensory pathways.Chem Senses2017,42:375-379.
3.Padmanabhan K,Osakada F,Tarabrina A,Kizer E,Callaway EM,Gage FH,et al.Diverse representations of olfactory information in centrifugal feedback projections.J Neurosci2016,36:7535-7545.
4.D’Souza RD,Vijayaraghavan S.Paying attention to smell:cholinergic signaling in the olfactory bulb.Front Synaptic Neurosci 2014,6:21.
5.Fletcher ML,Chen WR.Neural correlates of olfactory learning:Critical role of centrifugal neuromodulation.Learn Mem 2010,17:561-570.
6.Markopoulos F,Rokni D,Gire DH,Murthy VN.Functional properties of cortical feedback projections to the olfactory bulb.Neuron 2012,76:1175-1188.
7.Imai T.Construction of functional neuronal circuitry in the olfactory bulb.Semin Cell Dev Biol 2014,35:180-188.
8.Uchida N,Poo C,Haddad R.Coding and transformations in the olfactory system.Annu Rev Neurosci 2014,37:363-385.
9.Takahashi H,Ogawa Y,Yoshihara S,Asahina R,Kinoshita M,Kitano T,et al.A subtype of olfactory bulb interneurons is required for odor detection and discrimination behaviors.J Neurosci 2016,36:8210-8227.
10.Grimaud J,Lledo PM.Illuminating odors:when optogenetics brings to light unexpected olfactory abilities.Learn Mem 2016,23:249-254.
11.Oswald AM,Urban NN.There and back again:the corticobulbar loop.Neuron 2012,76:1045-1047.
12.Otazu GH,Chae H,Davis MB,Albeanu DF.Cortical feedback decorrelates olfactory bulb output in awake mice.Neuron 2015,86:1461-1477.
13.Linster C,Cleland TA.Neuromodulation of olfactory transformations.Curr Opin Neurobiol 2016,40:170-177.
14.Lizbinski KM,Dacks AM.Intrinsic and extrinsic neuromodulation of olfactory processing.Front Cell Neurosci 2017,11:424.
15.Rothermel M,Wachowiak M.Functional imaging of cortical feedback projections to the olfactory bulb.Front Neural Circuits2014,8:73.
16.Manella LC,Petersen N,Linster C.Stimulation of the locus ceruleus modulates signal-to-noise ratio in the olfactory bulb.J Neurosci 2017,37:11605-11615.
17.Case DT,Burton SD,Gedeon JY,Williams SG,Urban NN,Seal RP.Layer-and cell type-selective co-transmission by a basal forebrain cholinergic projection to the olfactory bulb.Nat Commun 2017,8:652.
18.Wachowiak M,Economo MN,Diaz-Quesada M,Brunert D,Wesson DW,White JA,et al.Optical dissection of odor information processing in vivo using GCaMPs expressed in specified cell types of the olfactory bulb.J Neurosci 2013,33:5285-5300.
19.Burton SD.Inhibitory circuits of the mammalian main olfactory bulb.J Neurophysiol 2017,118:2034-2051.
20.Luo L,Callaway EM,Svoboda K.Genetic dissection of neural circuits.Neuron 2008,57:634-660.
21.Thorne RG,Emory CR,Ala TA,Frey WH,2nd.Quantitative analysis of the olfactory pathway for drug delivery to the brain.Brain Res 1995,692:278-282.
22.Callaway EM.Transneuronal circuit tracing with neurotropic viruses.Curr Opin Neurobiol 2008,18:617-623.
23.Nassi JJ,Cepko CL,Born RT,Beier KT.Neuroanatomy goes viral!Front Neuroanat 2015,9:80.
24.Bienkowski MS,Wendel ES,Rinaman L.Organization of multisynaptic circuits within and between the medial and the central extended amygdala.J Comp Neurol 2013,521:3406-3431.
25.Callaway EM,Luo L.Monosynaptic circuit tracing with glycoprotein-deleted rabies viruses.J Neurosci 2015,35:8979-8985.
26.Willhite DC,Nguyen KT,Masurkar AV,Greer CA,Shepherd GM,Chen WR.Viral tracing identifies distributed columnar organization in the olfactory bulb.Proc Natl Acad Sci USA 2006,103:12592-12597.
27.Kikuta S,Sato K,Kashiwadani H,Tsunoda K,Yamasoba T,Mori K.From the Cover:Neurons in the anterior olfactory nucleus pars externa detect right or left localization of odor sources.Proc Natl Acad Sci USA 2010,107:12363-12368.
28.Esquivelzeta Rabell J,Mutlu K,Noutel J,Martin Del Olmo P,Haesler S.Spontaneous rapid odor source localization behavior requires interhemispheric communication.Curr Biol 2017,27:1542-1548 e1544.
29.Wilson DA,Sullivan RM.Cortical processing of odor objects.Neuron 2011,72:506-519.
30.Tye KM,Deisseroth K.Optogenetic investigation of neural circuits underlying brain disease in animal models.Nat Rev Neurosci 2012,13:251-266.
31.Spehr M,Spehr J,Ukhanov K,Kelliher KR,Leinders-Zufall T,Zufall F.Parallel processing of social signals by the mammalian main and accessory olfactory systems.Cell Mol Life Sci 2006,63:1476-1484.
32.Sewards TV,Sewards MA.Input and output stations of the entorhinal cortex:superficial vs.deep layers or lateral vs.medial divisions?Brain Res Brain Res Rev 2003,42:243-251.
33.Shipley MT,Ennis M.Functional organization of olfactory system.J Neurobiol 1996,30:123-176.
34.Ke MT,Fujimoto S,Imai T.SeeDB:a simple and morphologypreserving optical clearing agent for neuronal circuit reconstruction.Nat Neurosci 2013,16:1154-1161.
35.De Saint Jan D,Hirnet D,Westbrook GL,Charpak S.External tufted cells drive the output of olfactory bulb glomeruli.J Neurosci 2009,29:2043-2052.
36.Liu S,Plachez C,Shao Z,Puche A,Shipley MT.Olfactory bulb short axon cell release of GABA and dopamine produces a temporally biphasic inhibition-excitation response in external tufted cells.J Neurosci 2013,33:2916-2926.
37.Kiyokage E,Pan YZ,Shao Z,Kobayashi K,Szabo G,Yanagawa Y,et al.Molecular identity of periglomerular and short axon cells.J Neurosci 2010,30:1185-1196.
38.Gire DH,Franks KM,Zak JD,Tanaka KF,Whitesell JD,Mulligan AA,et al.Mitral cells in the olfactory bulb are mainly excited through a multistep signaling path.J Neurosci 2012,32:2964-2975.
39.Murphy GJ,Darcy DP,Isaacson JS.Intraglomerular inhibition:signaling mechanisms of an olfactory microcircuit.Nat Neurosci2005,8:354-364.
40.Najac M,Sanz Diez A,Kumar A,Benito N,Charpak S,De Saint Jan D.Intraglomerular lateral inhibition promotes spike timing variability in principal neurons of the olfactory bulb.J Neurosci2015,35:4319-4331.
41.Parsa PV,D’Souza RD,Vijayaraghavan S.Signaling between periglomerular cells reveals a bimodal role for GABA in modulating glomerular microcircuitry in the olfactory bulb.Proc Natl Acad Sci U S A 2015,112:9478-9483.
42.Liu S,Puche AC,Shipley MT.The interglomerular circuit potently inhibits olfactory bulb output neurons by both direct and indirect pathways.J Neurosci 2016,36:9604-9617.
43.Banerjee A,Marbach F,Anselmi F,Koh MS,Davis MB,Garcia da Silva P,et al.An interglomerular circuit gates glomerular output and implements gain control in the mouse olfactory bulb.Neuron 2015,87:193-207.
44.Burton SD,LaRocca G,Liu A,Cheetham CE,Urban NN.Olfactory bulb deep short-axon cells mediate widespread inhibition of tufted cell apical dendrites.J Neurosci 2017,37:1117-1138.
45.Eyre MD,Antal M,Nusser Z.Distinct deep short-axon cell subtypes of the main olfactory bulb provide novel intrabulbar and extrabulbar GABAergic connections.J Neurosci 2008,28:8217-8229.
46.Pressler RT,Strowbridge BW.Blanes cells mediate persistent feedforward inhibition onto granule cells in the olfactory bulb.Neuron 2006,49:889-904.
47.Eyre MD,Kerti K,Nusser Z.Molecular diversity of deep shortaxon cells of the rat main olfactory bulb.Eur J Neurosci 2009,29:1397-1407.
48.Kelsch W,Sim S,Lois C.Watching synaptogenesis in the adult brain.Annu Rev Neurosci 2010,33:131-149.
49.Belluscio L,Lodovichi C,Feinstein P,Mombaerts P,Katz LC.Odorant receptors instruct functional circuitry in the mouse olfactory bulb.Nature 2002,419:296-300.
50.Lodovichi C,Belluscio L,Katz LC.Functional topography of connections linking mirror-symmetric maps in the mouse olfactory bulb.Neuron 2003,38:265-276.
51.Brunjes PC,Illig KR,Meyer EA.A field guide to the anterior olfactory nucleus(cortex).Brain Res Brain Res Rev 2005,50:305-335.
52.Yan Z,Tan J,Qin C,Lu Y,Ding C,Luo M.Precise circuitry links bilaterally symmetric olfactory maps.Neuron 2008,58:613-624.
53.Illig KR,Eudy JD.Contralateral projections of the rat anterior olfactory nucleus.J Comp Neurol 2009,512:115-123.
54.Boyd AM,Sturgill JF,Poo C,Isaacson JS.Cortical feedback control of olfactory bulb circuits.Neuron 2012,76:1161-1174.
55.Insausti R,Herrero MT,Witter MP.Entorhinal cortex of the rat:cytoarchitectonic subdivisions and the origin and distribution of cortical efferents.Hippocampus 1997,7:146-183.
56.de la Rosa-Prieto C,Ubeda-Banon I,Mohedano-Moriano A,ProSistiaga P,Saiz-Sanchez D,Insausti R,et al.Subicular and CA1hippocampal projections to the accessory olfactory bulb.Hippocampus 2009,19:124-129.
57.de Olmos J,Hardy H,Heimer L.The afferent connections of the main and the accessory olfactory bulb formations in the rat:an experimental HRP-study.J Comp Neurol 1978,181:213-244.
58.van Groen T,Wyss JM.Extrinsic projections from area CA1 of the rat hippocampus:olfactory,cortical,subcortical,and bilateral hippocampal formation projections.J Comp Neurol 1990,302:515-528.
59.Devore S,de Almeida L,Linster C.Distinct roles of bulbar muscarinic and nicotinic receptors in olfactory discrimination learning.J Neurosci 2014,34:11244-11260.
60.Bendahmane M,Ogg MC,Ennis M,Fletcher ML.Increased olfactory bulb acetylcholine bi-directionally modulates glomerular odor sensitivity.Sci Rep 2016,6:25808.
61.Hamamoto M,Kiyokage E,Sohn J,Hioki H,Harada T,Toida K.Structural basis for cholinergic regulation of neural circuits in the mouse olfactory bulb.J Comp Neurol 2017,525:574-591.
62.Gracia-Llanes FJ,Crespo C,Blasco-Ibanez JM,Nacher J,Varea E,Rovira-Esteban L,et al.GABAergic basal forebrain afferents innervate selectively GABAergic targets in the main olfactory bulb.Neuroscience 2010,170:913-922.
63.Nunez-Parra A,Maurer RK,Krahe K,Smith RS,Araneda RC.Disruption of centrifugal inhibition to olfactory bulb granule cells impairs olfactory discrimination.Proc Natl Acad Sci U S A 2013,110:14777-14782.
64.Escanilla O,Arrellanos A,Karnow A,Ennis M,Linster C.Noradrenergic modulation of behavioral odor detection and discrimination thresholds in the olfactory bulb.Eur J Neurosci2010,32:458-468.
65.Escanilla O,Alperin S,Youssef M,Ennis M,Linster C.Noradrenergic but not cholinergic modulation of olfactory bulb during processing of near threshold concentration stimuli.Behav Neurosci 2012,126:720-728.
66.Doucette W,Milder J,Restrepo D.Adrenergic modulation of olfactory bulb circuitry affects odor discrimination.Learn Mem2007,14:539-547.
67.Li G,Linster C,Cleland TA.Functional differentiation of cholinergic and noradrenergic modulation in a biophysical model of olfactory bulb granule cells.J Neurophysiol 2015,114:3177-3200.
68.Zhou FW,Dong HW,Ennis M.Activation of beta-noradrenergic receptors enhances rhythmic bursting in mouse olfactory bulb external tufted cells.J Neurophysiol 2016,116:2604-2614.
69.Gire DH,Schoppa NE.Long-term enhancement of synchronized oscillations by adrenergic receptor activation in the olfactory bulb.J Neurophysiol 2008,99:2021-2025.
70.Zhong W,Li Y,Feng Q,Luo M.Learning and stress shape the reward response patterns of serotonin neurons.J Neurosci 2017,37:8863-8875.
71.Fonseca MS,Murakami M,Mainen ZF.Activation of dorsal raphe serotonergic neurons promotes waiting but is not reinforcing.Curr Biol 2015,25:306-315.
72.Liu ZX,Zhou JF,Li Y,Hu F,Lu Y,Ma M,et al.Dorsal raphe neurons signal reward through 5-HT and glutamate.Neuron2014,81:1360-1374.
73.Liu Y,Jiang Y,Si Y,Kim JY,Chen ZF,Rao Y.Molecular regulation of sexual preference revealed by genetic studies of5-HT in the brains of male mice.Nature 2011,472:95-99.
74.Kraus C,Castren E,Kasper S,Lanzenberger R.Serotonin and neuroplasticity-Links between molecular,functional and structural pathophysiology in depression.Neurosci Biobehav Rev 2017,77:317-326.
75.Luo MM,Li Y,Zhong WX.Do dorsal raphe 5-HT neurons encode‘‘beneficialness’’?Neurobiol Learn Mem 2016,135:40-49.
76.Miyazaki KW,Miyazaki K,Tanaka KF,Yamanaka A,Takahashi A,Tabuchi S,et al.Optogenetic activation of dorsal raphe serotonin neurons enhances patience for future rewards.Curr Biol2014,24:2033-2040.
77.Huang Z,Thiebaud N,Fadool DA.Differential serotonergic modulation across the main and accessory olfactory bulbs.J Physiol 2017,595:3515-3533.
78.Steinfeld R,Herb JT,Sprengel R,Schaefer AT,Fukunaga I.Divergent innervation of the olfactory bulb by distinct raphe nuclei.J Comp Neurol 2015,523:805-813.
79.Liu SL,Aungst JL,Puche AC,Shipley MT.Serotonin modulates the population activity profile of olfactory bulb external tufted cells.J Neurophysiol 2012,107:473-483.
80.Brill J,Shao Z,Puche AC,Wachowiak M,Shipley MT.Serotonin increases synaptic activity in olfactory bulb glomeruli.J Neurophysiol 2016,115:1208-1219.
81.Schmidt LJ,Strowbridge BW.Modulation of olfactory bulb network activity by serotonin:synchronous inhibition of mitral cells mediated by spatially localized GABAergic microcircuits.Learn Mem 2014,21:406-416.
82.Petzold GC,Hagiwara A,Murthy VN.Serotonergic modulation of odor input to the mammalian olfactory bulb.Nat Neurosci2009,12:784-791.
83.Brunert D,Tsuno Y,Rothermel M,Shipley MT,Wachowiak M.Cell-type-specific modulation of sensory responses in olfactory bulb circuits by serotonergic projections from the raphe nuclei.J Neurosci 2016,36:6820-6835.